Poirotte, C. | Search bioRxiv

bioRxiv2022

Primate mothers promote proximity between their offspring and infants who look like them

Behavioral discrimination of kin is a key process structuring social relationships in animals. In this study, we provide a first example of discrimination towards non-kin by third-parties through a mechanism of phenotype matching. In mandrills, we recently demonstrated increased facial resemblance among paternally-related juvenile and adult females indicating adaptive opportunities for paternal kin recognition. Here, we hypothesize that mothers use offsprings facial resemblance with other infants to guide offsprings social opportunities towards similarly-looking ones. Using deep learning for face recognition in 80 wild mandrill infants, we first show that infants born to the same father or conceived during the tenure of the same alpha male resemble each other the most, independently of their age, sex or maternal origin, extending previous results to the youngest age class. Using long-term behavioral observations on association patterns and controlling for matrilineal origin, maternal relatedness and infant age and sex, we then demonstrate that, as hypothesized, mothers are spatially closer to infants that resemble their own offspring more, thereby facilitating associations among similar-looking infants. Using theoretical modeling, we describe a plausible evolutionary process whereby mothers gain fitness benefits by promoting nepotism among paternally related infants. This mechanism, that we call "second-order kin selection", may extend beyond mother-infant interactions and has the potential to explain cooperative behaviors among non-kin in social species, including humans.

evolutionary biology↗

bioRxiv2019

Same father, same face: deep-learning reveals paternally-derived signalling of kinship in a wild primate

Animal faces convey important information such as individual health status1 or identity2,3. Human and nonhuman primates rely on highly heritable facial traits4,5 to recognize their kin6-8. However, whether these facial traits have evolved for this specific function of kin recognition remains unknown. We present the first unambiguous evidence that inter-individual facial similarity has been selected to signal kinship using a state-of-the-art artificial intelligence approach based on deep neural networks and long-term data on a natural population of nonhuman primates. The typical matrilineal society of mandrills, is characterized by an extreme males reproductive skew with one male generally siring the large majority of offspring born into the different matrilines each year9. Philopatric females are raised and live throughout their lives with familiar maternal half-sisters (MHS) but because of males reproductive monopolization, they also live with unfamiliar paternal half-sisters (PHS). Because kin selection predicts differentiated interactions with kin rather than nonkin10 and that PHS largely outnumber MHS in a mandrills social group, natural selection should favour mechanisms to recognize PHS. Here, we first show that PHS socially interact with each other as much as MHS do, both more than nonkin. Second, using artificial intelligence trained to recognize individual mandrills from a database of 16k portrait pictures, we demonstrate that facial similarity increases with genetic relatedness. However, PHS resemble more to each other than MHS do, despite both kin categories sharing similar degrees of genetic relatedness. We propose genomic imprinting as a plausible genetic mechanism to explain paternally-derived facial similarity among PHS selected to improve kin recognition. This study further highlights the potential of artificial intelligence to study evolutionary mechanisms driving variation between phenotypes.

evolutionary biology↗